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Population Genetics of Bryophytes in Relation to Their Reproductive Biology

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Population Genetics of Bryophytes in Relation to Their Reproductive Biology J. Hattori Bot. Lab. No. 76: 147- 157 (Oct. 1994) POPULATION GENETICS OF BRYOPHYTES IN RELATION TO THEIR REPRODUCTIVE BIOLOGY ROBERT WYATT1 ABSTRACT. Several unusual features of bryophyte reproduction lead to predictions about levels of genetic variation and its partitioning among natural populations. Dominance of the life cycle by a free-living, haploid gametophyte suggests that levels of genetic variation should be low. lsozyme data indicate, however, that mosses display a range of variation comparable to that observed for diploid plants. The range for liverworts is less. Because of the tight coupling of ploidy level and sexuality in most bryophytes, it is difficult to determine if levels of genetic variation are higher in unisexual than in bisexual taxa. Bisexual allopolyploids in Plagiomnium and Rhizomnium typically show fixed heterozygosity, which inflates their gene diversity statistics relative to their unisexual, haploid congeners. Nevertheless, gene diversities are also higher for bisexual, haploid species of Plagiothecium than for their unisexual, haploid relatives. There are also few data available to test the prediction of higher rates of self-fertilization and greater differentiation among populations of bisexual than of unisexual mosses and liverworts. Restricted gene flow due to short sperm dispersal distances should lead to strong differentiation among populations, but this may be counteracted by long-distance dispersal of spores. Typically degrees of genetic differentiation among conspecific populations of bryophytes are similiar to those observed in seed plants, except that intercontinentally disj unct populations of bryophytes often are only weakly differentiated. Asexual reproduction is common and widespread in bryophytes and appears to lead to large clonal patches in some taxa. The recent discovery of several allopolyploid bryophytes suggests that interspecific hybridization is more common than has been thought. This conclusion fits better with the limited possibilities of bryophytes with respect to reproductive isolation, given that fertilization is external and effected by water in all taxa. INTRODUCTION Reproduction in bryophytes is most similar to the situation prevailing in the pteridophytes. The most salient features include: ( 1) sexual reproduction is accom­ plished by free-living gametophytes; (2) fertilization is effected by motile sperms that are released into free water; (3) intragametophytic self-fertilization is possible in species with bisexual gametophytes; ( 4) spores are typically small and may be carried long distances by the wind; and (5) asexual reproduction is widespread and common. The ferns and fern allies share all of these features with mosses, liverworts, and hornworts. The major differences between these two groups of land plants flow from the fact that the sporophyte generation is relatively reduced in size and importance in the bryophyte life cycle. Thus, most of the asexual processes in pteridophytes involve propagation of sporophytes. Another important distinction is that, whereas most pteridophytes are potentially bisexual, 60-70% of all bryophytes are unisexual (Wyatt and Anderson 1984). 1 Institute of Ecology, University of Georgia, Athens, Georgia 30602, U.S.A. 148 J. Hattori Bot. Lab. No. 76 I 9 9 4 PREDICTIONS Given the characteristic features of bryophyte reproduction, it is possible to predict their effect on the population genetics of these plants. ( l) Natural selection, acting directly on the haploid genotype of bryophyte gametophytes, should lead to reduced levels of genetic variation. Because new genetic variants that arise by mutation are immediately expressed, natural selection should eliminate them very quickly, even if they are only mildly deleterious. Unlike diploid plants and animals, in which deleterious alleles can be sheltered in the heterozygous state, all genetic variants within haploid gametophytes are exposed. Among others, Mulcahy ( 1979) has argued that intense selection on gametophytes of angiosperms (i.e., pollen tubes) has been of primary importance in the rise of the flowering plants to dominance. Szweykowski ( 1984) has pointed out that bryophyte populations should be likened to arrays of gametes in other land plants and has suggested that some unusual properties of moss and liverwort populations may derive from their unique structure. There are some basic differences of opinion regarding the base number of chromo­ somes for mosses and liverworts and, therefore, whether the genomes of gametophytic plants are truly haploid. Schuster ( 1966) and Newton (1983) believe that modern liverworts are ancient polyploids built up from a base number of x = 4 or 5. On the other hand, Smith (1978) and Crosby ( 1980) contend that the base number is x = 8- 10. For most mosses it seems likely that the base number is x = 6 or 7 (Smith 1978; Anderson 1980). This is consistent with all isozyme studies to date, which have reported simple haploid patterns of expression in taxa at the presumed base level. Thus, it appears that arguments predicated on natural selection acting on functionally haploid genotypes in bryophytes are appropriate for these taxa. (2) Some mosses and liverworts are capable of producing bisexual gametophytes. This creates a situation in which there are three possibilities with respect to mating: ( l) there can be intergametophytic crossing, cross-fertilization of gametophytes produced by different sporophytes, which is analogous to outcrossing in seed plants; (2) there can be intergametophytic selfing, cross-fertilization of gametophytes produced by the same sporophyte, which is analogous to selfing in seed plants; and (3) there can be intragametophytic selfing, self-fertilization of a single gametophyte, which is a mating possibility unique to bryophytes and homosporous pteridophytes and which results in a diploid sporophyte that is homozygous at all loci. In most bryophytes, however, this third possibility is eliminated by unisexuality. According to Wyatt and Anderson ( 1984 ), approximately 60% of mosses and 70% of liverworts are unisexual, and even among bisexual species there may be mechanisms that favor cross-fertilization between gametophytes. Nevertheless, to the extent that self-fertilization does occur more frequently in bisexual than in unisexual mosses and liverworts, we can predict higher rates of inbreeding. This, in turn, should result in significant genetic substructuring of popula­ tions. Moreover, inbreeding species should partition relatively more of their genetic variation among, rather than within, populations. There should be greater potential for R. WYATT: Population genetics of bryophytes in relation to their reproductive biology 149 racial differentiation across the species range. (3) Gene flow in bryophytes is effected during sexual reproduction by dispersal of sperms and of spores. All recent reviews of sperm dispersal in mosses and liverworts have reached the same conclusion: sperm dispersal distances are very short (Wyatt & Anderson 1983). Even in larger species with splash cups, only rarely do sperms get dispersed more than 50cm. In species without splash cups, fertilization typically occurs within a radius of about 10 cm. Many authors have assumed that the spores of bryophytes are capable of long­ distance transport by the wind. It is certainly true that many moss and liverwort species are very widely distributed. Detailed studies attempting to quantify spore dispersal from natural populations, however, have documented that deposition declines pre­ cipitously as a function of distance from the source (Miles & Longton 1990, 1992; Stoneburner et al. 1992). Nevertheless, spores are produced in prodigious numbers and typically only a small fraction are trapped; thus, it is possible that many escape and travel long distances to establish new colonies remote from the source. To the extent that gene flow, presumably almost entirely by spores or asexual fragments, is extensive between populations of bryophytes, we should expect popula­ tions to be relatively homogeneous across their ranges. If effective gene flow is more restricted, we predict that populations will be more strongly differentiated. If gene flow is very strongly limited, we might even expect to find genetic substructuring within populations from a single site. ( 4) In addition to the many and diverse forms of specialized asexual propagules, it appears that most, if not all, bryophytes are capable of asexual reproduction by regeneration of unspecialized fragments of the gametophytic thallus. In many cases it appears that asexual progagules are resistant to the perils of long-distance transport and may be carried great distances. On the other hand, they probably are also very important in increasing local poplation size (Wyatt 1982). To the extent that local populations of bryophytes increase in size by recruitment of clonal individuals, we should expect overall gene diversity to decrease. This would be especially true if certain genotypes were more successful than others at asexual reproduction. Over time local populations might come to be dominated by one or a few highly successful genotypes. On a larger scale, asexual reproduction would have much the same effect as inbreeding: enhancing levels of genetic differentation among popula­ tions across the species range. This effect might be counteracted, however, if asexual propagules were highly dispersible and tended to increase rates of gene flow between populations. (5) Unlike seed plants, which have
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